"Phoenix in Flight": an unique fruit morphology ensures wind dispersal of seeds of the phoenix tree (Firmiana simplex (L.) W. Wight)

Abstract

Background: Many seed plants produce winged diaspores that use wind to disperse their seeds. The morphology of these diaspores is directly related to the seed dispersal potential. The majority of winged diaspores have flat wings and only seeds; however, some angiosperms, such as Firmiana produce winged fruit with a different morphology, whose seed dispersal mechanisms are not yet fully understood. In this study, we observed the fruit development of F. simplex and determined the morphological characteristics of mature fruit and their effects on the flight performance of the fruit.

Results: We found that the pericarp of F. simplex dehisced early and continued to unfold and expand during fruit development until ripening, finally formed a spoon-shaped wing with multiple alternate seeds on each edge. The wing caused mature fruit to spin stably during descent to provide a low terminal velocity, which was correlated with the wing loading and the distribution of seeds on the pericarp. When the curvature distribution of the pericarp surface substantially changed, the aerodynamic characteristics of fruit during descent altered, resulting in the inability of the fruit to spin.

Conclusions: Our results suggest that the curved shape and alternate seed distribution are necessary for the winged diaspore of F. simplex to stabilize spinning during wind dispersal. These unique morphological characteristics are related to the early cracking of fruits during development, which may be an adaptation for the wind dispersal of seeds.

Keywords: Curved surface; Firmiana; Flight performance; Fruit development; Spinning; Wind dispersal.

Fig. 1

Development of the fruit of Firmiana simplex. a An immature fruit developing on the tree. b The morphology of the fruitlet at different developmental stages from flowering to fruit ripening. The middle inset shows a mature aggregate fruit. The coloured curves indicate the different stages of fruit development: green, before fruit cracking; yellow, fruit cracking and expanding; orange, fruit drying. The values on the curves indicate the duration of each stage. c The internal structure of pericarps at several different stages of fruit development. The numbers correspond to different developmental stages in (b)

Fig. 2

Morphological characteristics of the fruit of Firmiana simplex. a Pericarp projected area, seed number, total mass, and wing loading of the fruit with different lengths. Scattered points represent different fruit samples in each graph, and the straight lines are the linear fitting curves of the data. b The distribution of seed positions on the pericarp. Coloured circles represent the different seeds in the fruit. Hollow circles and solid circles correspond to seeds starting from the left and right sides of the pericarp along the long axis, respectively. c The curvature distribution of the pericarp surface. The ventral surface of the pericarp points inward

Fig. 3

Terminal descent velocity versus number of seeds (a) and wing loading (b) in Firmiana simplex. Solid points and hollow points represent two groups of fruit spinning with their dorsal and ventral sides downward, respectively, and the solid lines and dotted lines are the linear fitting curves of these two groups of data, respectively

Fig. 4

Flight-attitude changes of fruit during falling in Firmiana simplex. a Experimental samples of actual fruit and paper models containing only one seed per fruit. b Posture changes of experimental samples during falling. The coloured bars represent different postures: green, downward acceleration; yellow, tumbling; orange, decelerated spinning; red, stable spinning; black, falling in a near straight line. The number 0 identifies the actual fruit and other sequential numbers identify different paper models: 1, Model I, in which the surface curvature of all areas were similar to the actual pericarp; 2, Model II, in which the curvature of the ovary area was similar to the actual pericarp but the top area was flat; 3, Model III, in which the curvature of the top was similar to the actual pericarp but the ovary area was flat; 4, Model IV, in which all areas were flat

Fig. 5

Results of aerodynamics simulation of a static pericarp in Firmiana simplex. a 3D models of pericarps in digital simulation. The sequential numbers identify the pericarp corresponding to the shape of different paper models. b Streamline distributions in the long axis section of pericarp models. c Pressure distributions on the long axis section of pericarp models